Reducing inequities in colorectal cancer screening in North America

Journal of Carcinogenesis

Volumn 13, Issue 1, 2014, Pages

  Decker, Kathleen ^a,b   Singh, Harminder ^a,b  

^a UNIVERSITY OF MANITOBA   (Canada)

^b Cancer Care Manitoba ^*  (Canada)

Author keywords

Cancer; colorectal; equity; participation; screening

Indexed keywords

EID: 85002170013     PISSN: 09746773     EISSN: 14773163     Source Type: Journal    
DOI: 10.4103/1477-3163.144576     Document Type: Review

References (112)

1. Canadian Cancer Society's Steering Committee on Cancer Statistics. Canadian Cancer Statistics 2013. Toronto, ON: Canadian Cancer Society; 2013.
2. Surveillance, Epidemiology, and End Results (SEER) Program, National Cancer Institute. SEER Stat Fact Sheets: Colon and Rectum Cancer; 2014. [Last accessed on August 15, 2014].
3. Wilson LS, Lightwood J. Model of estimated rates of colorectal cancer from polyp growth by year of surveillance. J Med Screen 2001;8:187-96.
4. Kreuter MW, Garibay LB, Pfeiffer DJ, Morgan JC, Thomas M, Wilson KM, et al. Small media and client reminders for colorectal cancer screening: Current use and gap areas in CDC's Colorectal Cancer Control Program. Prev Chronic Dis 2012;9:E1-31.
5. Canadian Partnership Against Cancer. Colorectal Cancer Screening in Canada: Program Performance Results Report, January 2009 to December 2011. Toronto, ON: Canadian Partnership Against Screening; 2013.
6. Kewenter J, Brevinge H, Engarås B, Haglind E, Ahrén C. Results of screening, rescreening, and follow-up in a prospective randomized study for detection of colorectal cancer by fecal occult blood testing. Results for 68, 308 subjects. Scand J Gastroenterol 1994;29:468-73.
7. Hardcastle JD, Chamberlain JO, Robinson MH, Moss SM, Amar SS, Balfour TW, et al. Randomised controlled trial of faecal-occult-blood screening for colorectal cancer. Lancet 1996;348:1472-7.
8. Jørgensen OD, Kronborg O, Fenger C. A randomised study of screening for colorectal cancer using faecal occult blood testing: Results after 13 years and seven biennial screening rounds. Gut 2002;50:29-32.
9. Kronborg O, Jørgensen OD, Fenger C, Rasmussen M. Randomized study of biennial screening with a faecal occult blood test: Results after nine screening rounds. Scand J Gastroenterol 2004;39:846-51.
10. Mandel JS, Bond JH, Church TR, Snover DC, Bradley GM, Schuman LM, et al. Reducing mortality from colorectal cancer by screening for fecal occult blood. Minnesota Colon Cancer Control Study. N Engl J Med 1993;328:1365-71.
11. Hewitson P, Glasziou P, Watson E, Towler B, Irwig L. Cochrane systematic review of colorectal cancer screening using the fecal occult blood test (hemoccult): An update. Am J Gastroenterol 2008;103:1541-9.
12. Shaukat A, Mongin SJ, Geisser MS, Lederle FA, Bond JH, Mandel JS, et al. Long-term mortality after screening for colorectal cancer. N Engl J Med 2013;369:1106-14.
13. van Rossum LG, Van Rijn AF, Laheij R, van Oijen MG, Flockens P, van Krieken HH, et al. Random comparison of guaiac and immunochemical fecal occult blood tests for colorectal cancer in a screening population. Gastroenterol 2008;135 (1):82-90.
14. Hol L, van Leerdam ME, van Ballegooijen M, van Vuuren AJ, van Dekken H, Reijerink JC, et al. Screening for colorectal cancer: Randomised trial comparing guaiac-based and immunochemical faecal occult blood testing and flexible sigmoidoscopy. Gut 2010;59:62-8.
15. Atkin WS, Edwards R, Kralj-Hans I, Wooldrage K, Hart AR, Northover JM, et al. Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: A multicentre randomised controlled trial. Lancet 2010;375:1624-33.
16. Schoen RE, Pinsky PF, Weissfeld JL, Yokochi LA, Church T, Laiyemo AO, et al. Colorectal-cancer incidence and mortality with screening flexible sigmoidoscopy. N Engl J Med 2012;366:2345-57.
17. Elmunzer BJ, Hayward RA, Schoenfeld PS, Saini SD, Deshpande A, Waljee AK. Effect of flexible sigmoidoscopy-based screening on incidence and mortality of colorectal cancer: A systematic review and meta-analysis of randomized controlled trials. PLoS Med 2012;9:e1001352.
18. Holme Ø, Løberg M, Kalager M, Bretthauer M, Hernán MA, Aas E, et al. Effect of flexible sigmoidoscopy screening on colorectal cancer incidence and mortality: A randomized clinical trial. JAMA 2014;312:606-15.
19. Steele CB, Rim SH, Joseph DA, King JB, Seeff LC, Centers for Disease Control and Prevention (CDC). Colorectal cancer incidence and screening-United States, 2008 and 2010. MMWR Surveill Summ 2013;62 Suppl 3:53-60.
20. Singh H, Demers AA, Xue L, Turner D, Bernstein CN. Time trends in colon cancer incidence and distribution and lower gastrointestinal endoscopy utilization in Manitoba. Am J Gastroenterol 2008;103:1249-56.
21. Brenner H, Stock C, Hoffmeister M. Effect of screening sigmoidoscopy and screening colonoscopy on colorectal cancer incidence and mortality: Systematic review and meta-analysis of randomised controlled trials and observational studies. BMJ 2014;348:g2467.
22. Schmidt C. Colonoscopy vs sigmoidoscopy: New studies fuel ongoing debate. J Natl Cancer Inst 2012;104:1350-1.
23. Shapiro JA, Klabunde CN, Thompson TD, Nadel MR, Seeff LC, White A. Patterns of colorectal cancer test use, including CT colonography, in the 2010 National Health Interview Survey. Cancer Epidemiol Biomarkers Prev 2012;21:895-904.
24. Ontario Ministry of Health and Long-term Care. Ontario FOBT Project. Final Report. Toronto, ON: Ontario Ministry of Health and Long-term Care; 2006.
25. Brett AS. Flexible sigmoidoscopy for colorectal cancer screening: More evidence, persistent ironies. JAMA 2014;312:601-2.
26. Imperiale TF, Ransohoff DF, Itzkowitz SH, Levin TR, Lavin P, Lidgard GP, et al. Multitarget stool DNA testing for colorectal-cancer screening. N Engl J Med 2014;370:1287-97.
27. Halligan S, Wooldrage K, Dadswell E, Kralj-Hans I, von Wagner C, Edwards R, et al. Computed tomographic colonography versus barium enema for diagnosis of colorectal cancer or large polyps in symptomatic patients (SIGGAR): A multicentre randomised trial. Lancet 2013;381:1185-93.
28. Lieberman D. Screening for colorectal cancer in individuals at average risk: Current methods and emerging issues. JAMA Intern Med 2014;174:10-1.
29. Johnson CD, Chen MH, Toledano AY, Heiken JP, Dachman A, Kuo MD, et al. Accuracy of CT colonography for detection of large adenomas and cancers. N Engl J Med 2008;359:1207-17.
30. Leddin DJ, Enns R, Hilsden R, Plourde V, Rabeneck L, Sadowski DC, et al. Canadian association of gastroenterology position statement on screening individuals at average risk for developing colorectal cancer: 2010. Can J Gastroenterol 2010;24:705-14.
31. Canadian Task Force on Preventive Health Care. Colorectal cancer screening. JAMC 2001;25:206-8.
32. U.S. Preventive Services Task Force. Screening for Colorectal Cancer: Clinical Summary of U.S. Preventive Services Task Force Recommendation. AHRQ Publication No. 08-05124-EF-4; 2008.
33. Levin B, Lieberman DA, McFarland B, Andrews KS, Brooks D, Bond J, et al. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: A joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. Gastroenterology 2008;134:1570-95.
34. Canadian Partnership Against Cancer. The 2014 Cancer System Performance Report. Toronto, ON: Canadian Partnership Against Cancer; 2014.
35. Liss DT, Baker DW. Understanding current racial/ethnic disparities in colorectal cancer screening in the United States: The contribution of socioeconomic status and access to care. Am J Prev Med 2014;46:228-36.
36. Statistics Canada. Canadian Community Health Survey 3.1; 2009. Available from: http://cansim2.statcan.gc.ca.proxy2.lib.umanitoba.ca. [Last accessed on 2010 Jan 12].
37. Daley CM, James AS, Filippi M, Weir M, Braiuca S, Kaur B, et al. American Indian community leader and provider views of needs and barriers to colorectal cancer screening. J Health Dispar Res Pract 2012;5.
38. Javanparast S, Ward P, Young G, Wilson C, Carter S, Misan G, et al. How equitable are colorectal cancer screening programs which include FOBTs? A review of qualitative and quantitative studies. Prev Med 2010;50:165-72.
39. Klabunde CN, Vernon SW, Nadel MR, Breen N, Seeff LC, Brown ML. Barriers to colorectal cancer screening: A comparison of reports from primary care physicians and average-risk adults. Med Care 2005;43:939-44.
40. Wardle J, McCaffery K, Nadel M, Atkin W. Socioeconomic differences in cancer screening participation: Comparing cognitive and psychosocial explanations. Soc Sci Med 2004;59:249-61.
41. Niederdeppe J, Levy AG. Fatalistic beliefs about cancer prevention and three prevention behaviors. Cancer Epidemiol Biomarkers Prev 2007;16:998-1003.
42. Wardle J, Steptoe A. Socioeconomic differences in attitudes and beliefs about healthy lifestyles. J Epidemiol Community Health 2003;57:440-3.
43. Katz SJ, Hofer TP. Socioeconomic disparities in preventive care persist despite universal coverage. Breast and cervical cancer screening in Ontario and the United States. JAMA 1994;272:530-4.
44. Canadian Partnership Against Cancer. Examining Disparities in Cancer Control. A System Performance Special Report. Toronto, ON: Canadian Partnership Against Cancer; 2014.
45. Hatch SL, Dohrenwend BP. Distribution of traumatic and other stressful life events by race/ethnicity, gender, SES and age: A review of the research. Am J Community Psychol 2007;40:313-32.
46. Marmot M, Friel S, Bell R, Houweling TA, Taylor S, Commission on Social Determinants of Health. Closing the gap in a generation: Health equity through action on the social determinants of health. Lancet 2008;372:1661-9.
47. Wardle J, Jarvis MJ, Steggles N, Sutton S, Williamson S, Farrimond H, et al. Socioeconomic disparities in cancer-risk behaviors in adolescence: Baseline results from the Health and Behaviour in Teenagers Study (HABITS). Prev Med 2003;36:721-30.
48. Weitzman ER, Zapka J, Estabrook B, Goins KV. Risk and reluctance: Understanding impediments to colorectal cancer screening. Prev Med 2001;32:502-13.
49. Berkowitz Z, Hawkins NA, Peipins LA, White MC, Nadel MR. Beliefs, risk perceptions, and gaps in knowledge as barriers to colorectal cancer screening in older adults. J Am Geriatr Soc 2008;56:307-14.
50. Worthley DL, Cole SR, Esterman A, Mehaffey S, Roosa NM, Smith A, et al. Screening for colorectal cancer by faecal occult blood test: Why people choose to refuse. Intern Med J 2006;36:607-10.
51. Lo SH, Waller J, Wardle J, von Wagner C. Comparing barriers to colorectal cancer screening with barriers to breast and cervical screening: A population-based survey of screening-age women in Great Britain. J Med Screen 2013;20:73-9.
52. von Wagner C, Good A, Smith SG, Wardle J. Responses to procedural information about colorectal cancer screening using faecal occult blood testing: The role of consideration of future consequences. Health Expect 2012;15:176-86.
53. Robb K, Wardle J, Stubbings S, Ramirez A, Austoker J, Macleod U, et al. Ethnic disparities in knowledge of cancer screening programmes in the UK. J Med Screen 2010;17:125-31.
54. von Wagner C, Good A, Whitaker KL, Wardle J. Psychosocial determinants of socioeconomic inequalities in cancer screening participation: A conceptual framework. Epidemiol Rev 2011;33:135-47.
55. Coughlin SS, Thompson T. Physician recommendation for colorectal cancer screening by race, ethnicity, and health insurance status among men and women in the United States, 2000. Health Promot Pract 2005;6:369-78.
56. Cole SR, Young GP, Esterman A, Cadd B, Morcom J. A randomised trial of the impact of new faecal haemoglobin test technologies on population participation in screening for colorectal cancer. J Med Screen 2003;10:117-22.
57. Lee HY, Im H. Colorectal cancer screening among Korean American immigrants: Unraveling the influence of culture. J Health Care Poor Underserved 2013;24:579-98.
58. Born W, Engelman K, Greiner KA, Bhattacharya SB, Hall S, Hou Q, et al. Colorectal cancer screening, perceived discrimination, and low-income and trust in doctors: A survey of minority patients. BMC Public Health 2009;9:363.
59. Steinwachs D, Allen JD, Barlow WE, Duncan RP, Egede LE, Friedman LS, et al. National Institutes of Health state-of-the-science conference statement: Enhancing use and quality of colorectal cancer screening. Ann Intern Med 2010;152:663-7.
60. Wu Z, Penning MJ, Schimmele CM. Immigrant status and unmet health care needs. Can J Public Health 2005;96:369-73.
61. Lee MC. Knowledge, barriers, and motivators related to cervical cancer screening among Korean-American women. A focus group approach. Cancer Nurs 2000;23:168-75.
62. Lee J, Parsons GF, Gentleman JF. Falling short of Pap test guidelines. Health Rep 1998;10:9-19.
63. Maxwell CJ, Bancej CM, Snider J, Vik SA. Factors important in promoting cervical cancer screening among Canadian women: Findings from the 1996-97 National Population Health Survey (NPHS). Can J Public Health 2001;92:127-33.
64. Woltman KJ, Newbold KB. Immigrant women and cervical cancer screening uptake: A multilevel analysis. Can J Public Health 2007;98:470-5.
65. Perdue DG, Haverkamp D, Perkins C, Daley CM, Provost E. Geographic variation in colorectal cancer incidence and mortality, age of onset, and stage at diagnosis among American Indian and Alaska Native people, 1990-2009. Am J Public Health 2014;104 Suppl 3:S404-14.
66. Kliewer EV, Demers AA, Elias B, Hall M, Turner D, Musto G. Cancer Incidence Among Status First Nations in Manitoba, Canada. Winnipeg, MB. Unpublished manuscript; 2013.
67. Espey DK, Wu XC, Swan J, Wiggins C, Jim MA, Ward E, et al. Annual report to the nation on the status of cancer, 1975-2004, featuring cancer in American Indians and Alaska Natives. Cancer 2007;110:2119-52.
68. Steele CB, Cardinez CJ, Richardson LC, Tom-Orme L, Shaw KM. Surveillance for health behaviors of American Indians and Alaska Natives-findings from the behavioral risk factor surveillance system, 2000-2006. Cancer 2008;113:1131-41.
69. Department of Health and Ageing and AIHW. National Bowel Cancer Screening Program Monitoring Report, 2008. Canberra, Australia: Department of Health and Ageing and AIHW; 2008.
70. Brawarsky P, Brooks DR, Mucci LA, Wood PA. Effect of physician recommendation and patient adherence on rates of colorectal cancer testing. Cancer Detect Prev 2004;28:260-8.
71. Wee CC, McCarthy EP, Phillips RS. Factors associated with colon cancer screening: The role of patient factors and physician counseling. Prev Med 2005;41:23-9.
72. Seeff LC, Nadel MR, Klabunde CN, Thompson T, Shapiro JA, Vernon SW, et al. Patterns and predictors of colorectal cancer test use in the adult U.S. population. Cancer 2004;100:2093-103.
73. Martens P, Fransoo R, The Need to Know Team, Burland E, Prior H, Burchill C, et al. What Works? A First Look at Evaluating Manitoba's Regional Health Programs and Policies at the Population Level. Winnipeg, MB: Manitoba Centre for Health Policy; 2008.
74. Ackerson K, Preston SD. A decision theory perspective on why women do or do not decide to have cancer screening: Systematic review. J Adv Nurs 2009;65:1130-40.
75. Meissner HI, Breen N, Klabunde CN, Vernon SW. Patterns of colorectal cancer screening uptake among men and women in the United States. Cancer Epidemiol Biomarkers Prev 2006;15:389-94.
76. Canadian Partnership Against Cancer. The 2012 Cancer System Performance Report. Toronto, ON: Canadian Partnership Against Cancer; 2012.
77. Weiss JM, Smith MA, Pickhardt PJ, Kraft SA, Flood GE, Kim DH, et al. Predictors of colorectal cancer screening variation among primary-care providers and clinics. Am J Gastroenterol 2013;108:1159-67.
78. Decker K, Demers A, Chateau D, Musto G, Nugent Z, Lotocki R, et al. Papanicolaou test utilization and frequency of screening opportunities among women diagnosed with cervical cancer. Open Med 2009;3:e140-7.
79. Klabunde CN, Riley GF, Mandelson MT, Frame PS, Brown ML. Health plan policies and programs for colorectal cancer screening: A national profile. Am J Manag Care 2004;10:273-9.
80. Singh SM, Paszat LF, Li C, He J, Vinden C, Rabeneck L. Association of socioeconomic status and receipt of colorectal cancer investigations: A population-based retrospective cohort study. CMAJ 2004;171:461-5.
81. Cooper GS, Doug Kou T. Underuse of colorectal cancer screening in a cohort of Medicare beneficiaries. Cancer 2008;112:293-9.
82. Baron RC, Rimer BK, Breslow RA, Coates RJ, Kerner J, Melillo S, et al. Client-directed interventions to increase community demand for breast, cervical, and colorectal cancer screening a systematic review. Am J Prev Med 2008;35:S34-55.
83. Myers RE, Bittner-Fagan H, Daskalakis C, Sifri R, Vernon SW, Cocroft J, et al. A randomized controlled trial of a tailored navigation and a standard intervention in colorectal cancer screening. Cancer Epidemiol Biomarkers Prev 2013;22:109-17.
84. Myers RE, Sifri R, Hyslop T, Rosenthal M, Vernon SW, Cocroft J, et al. A randomized controlled trial of the impact of targeted and tailored interventions on colorectal cancer screening. Cancer 2007;110:2083-91.
85. Menon U, Belue R, Wahab S, Rugen K, Kinney AY, Maramaldi P, et al. A randomized trial comparing the effect of two phone-based interventions on colorectal cancer screening adherence. Ann Behav Med 2011;42:294-303.
86. Costanza ME, Luckmann R, Stoddard AM, White MJ, Stark JR, Avrunin JS, et al. Using tailored telephone counseling to accelerate the adoption of colorectal cancer screening. Cancer Detect Prev 2007;31:191-8.
87. Vernon SW, Bartholomew LK, McQueen A, Bettencourt JL, Greisinger A, Coan SP, et al. A randomized controlled trial of a tailored interactive computer-delivered intervention to promote colorectal cancer screening: Sometimes more is just the same. Ann Behav Med 2011;41:284-99.
88. Jerant A, Kravitz RL, Sohler N, Fiscella K, Romero RL, Parnes B, et al. Sociopsychological tailoring to address colorectal cancer screening disparities: A randomized controlled trial. Ann Fam Med 2014;12:204-14.
89. Bennett GG. Connecting eHealth with 2-1-1 to reduce health disparities. Am J Prev Med 2012;43:S509-11.
90. Grunfeld E, Manca D, Moineddin R, Thorpe KE, Hoch JS, Campbell-Scherer D, et al. Improving chronic disease prevention and screening in primary care: Results of the BETTER pragmatic cluster randomized controlled trial. BMC Fam Pract 2013;14:175.
91. Christie J, Itzkowitz S, Lihau-Nkanza I, Castillo A, Redd W, Jandorf L. A randomized controlled trial using patient navigation to increase colonoscopy screening among low-income minorities. J Natl Med Assoc 2008;100:278-84.
92. Lasser KE, Murillo J, Lisboa S, Casimir AN, Valley-Shah L, Emmons KM, et al. Colorectal cancer screening among ethnically diverse, low-income patients: A randomized controlled trial. Arch Intern Med 2011;171:906-12.
93. Lebwohl B, Neugut AI, Stavsky E, Villegas S, Meli C, Rodriguez O, et al. Effect of a patient navigator program on the volume and quality of colonoscopy. J Clin Gastroenterol 2011;45:e47-53.
94. Paskett ED, Harrop JP, Wells KJ. Patient navigation: An update on the state of the science. CA Cancer J Clin 2011;61:237-49.
95. Myers RE, Hyslop T, Sifri R, Bittner-Fagan H, Katurakes NC, Cocroft J, et al. Tailored navigation in colorectal cancer screening. Med Care 2008;46:S123-31.
96. Sarfaty M, Doroshenk M, Hotz J, Brooks D, Hayashi S, Davis TC, et al. Strategies for expanding colorectal cancer screening at community health centers. CA Cancer J Clin 2013;63:221-31.
97. PRA Inc. Evaluation of the Physician Integrated Network (PIN): Phase I Summary Report. Winnipeg, MB: Prairie Research Associates Inc.; 2009.
98. Manitoba Health. Manitoba's Physician Integrated Network (PIN) Initiative A Benefits Evaluation Report. Winnipeg, MB: Manitoba Health; 2012.
99. Benarroch-Gampel J, Sheffield KM, Lin YL, Kuo YF, Goodwin JS, Riall TS. Colonoscopist and primary care physician supply and disparities in colorectal cancer screening. Health Serv Res 2012;47:1137-57.
100. Swan J, Breen N, Coates RJ, Rimer BK, Lee NC. Progress in cancer screening practices in the United States: Results from the 2000 national health interview survey. Cancer 2003;97:1528-40.
101. Breslow RA, Rimer BK, Baron RC, Coates RJ, Kerner J, Wilson KM, et al. Introducing the community guide's reviews of evidence on interventions to increase screening for breast, cervical, and colorectal cancers. Am J Prev Med 2008;35:S14-20.
102. Taplin SH, Anhang Price R, Edwards HM, Foster MK, Breslau ES, Chollette V, et al. Introduction: Understanding and influencing multilevel factors across the cancer care continuum. J Natl Cancer Inst Monogr 2012;2012:2-10.
103. Task Force on Community Preventive Services. Recommendations for client-and provider-directed interventions to increase breast, cervical, and colorectal cancer screening. Am J Prev Med 2008;35:S21-5.
104. Clauser SB, Taplin SH, Foster MK, Fagan P, Kaluzny AD. Multilevel intervention research: Lessons learned and pathways forward. J Natl Cancer Inst Monogr 2012;2012:127-33.
105. Anhang Price R, Zapka J, Edwards H, Taplin SH. Organizational factors and the cancer screening process. J Natl Cancer Inst Monogr 2010;2010:38-57.
106. Potter MB. Strategies and resources to address colorectal cancer screening rates and disparities in the United States and globally. Annu Rev Public Health 2013;34:413-29.
107. Grubbs SS, Polite BN, Carney J Jr, Bowser W, Rogers J, Katurakes N, et al. Eliminating racial disparities in colorectal cancer in the real world: It took a village. J Clin Oncol 2013;31:1928-30.
108. Richards CA, Kerker BD, Thorpe L, Olson C, Krauskopf MS, Silver LS, et al. Increased screening colonoscopy rates and reduced racial disparities in the New York citywide campaign: An urban model. Am J Gastroenterol 2011;106:1880-6.
109. Green BB, Coronado GD, Devoe JE, Allison J. Navigating the murky waters of colorectal cancer screening and health reform. Am J Public Health 2014;104:982-6.
110. Raffle A, Gray M. Screening: Evidence and Practice. New York, NY: Oxford University Press; 2007.
111. Wilson JM, Jungner YG. Principles and practice of mass screening for disease. Bol Oficina Sanit Panam 1968;65:281-393.
112. Canadian Partnership Against Cancer. Quality Determinants and Indicators for Measuring Colorectal Cancer Screening Program Performance in Canada. Toronto, ON: Canadian Partnership Against Cancer; 2013.